Physical Exercise Introduced After Weaning Enhances Pancreatic Islet Responsiveness To Glucose And Potentiating Agents In Adult Msg-obese Rats

Physical exercise represents an alternative way to prevent and/or ameliorate chronic metabolic diseases. Disruption of sympathetic nervous system (SNS) activity contributes to adiposity in obese subjects. Here, we verified the preventive effect of swimming training upon adiposity, adrenal catecholamine storage, and pancreatic islet function in obese monosodium glutamate (MSG)-treated rats. Male neonatal Wistar rats received MSG (4 mg/g body weight) during the first 5 days of life and, at weaning, half of the rats were submitted to swimming training, 30 min/day, 3 days a week, until 90 days of age (exercised rats: MSGex). Half of the rats were used as controls (sedentary group, MSGsd). Exercise training (ET) decreased insulinemia and fat deposition in MSGex, and increased adrenal catecholamine content, compared with MSGsd rats. Insulinemia during the ivGTT was lower in MSGex rats, despite a lack of difference in glycemia. Swimming training enhanced insulin release in islets challenged by 2.8-8.3 mmol/l glucose, whereas, at supraphysiological glucose concentrations (11.1-16.7 mmol/l), MSGex islets secreted less insulin than MSGsd. No differences in insulin secretion were observed following l-arginine (Arg) or K+ stimuli. In contrast, islets from MSGex rats secreted more insulin when exposed to carbachol (100 μmol/l), forskolin (10 μmol/l), or IBMX (1 mmol/l) at 8.3 mmol/l glucose. Additionally, MSGex islets presented a better epinephrine inhibition upon insulin release. These results demonstrate that ET prevented the onset of obesity in MSG rats, probably by enhancing adrenal catecholamine levels. ET ameliorates islet responsiveness to several compounds, as well as insulin peripheral action. © Georg Thieme Verlag KG Stuttgart · New York.469609614Arrone, L.J., Mackintosh, R., Rosenbaum, M., Leibel, R.L., Hirsch, J., Cardiac autonomic nervous system activity in obese and never-obese young men (1997) Obes Res, 5, pp. 354-359Kahn, S.E., Prigeon, R.L., Schwartz, R.S., Fujimoto, W.Y., Knopp, R.H., Brunzell, J.D., Porte Jr., D., Obesity, body fat distribution, insulin sensitivity and Islet beta-cell function as explanations for metabolic diversity (2001) J Nutr, 131, pp. 354S-360SKahn, S.E., The relative contributions of insulin resistance and beta-cell dysfunction to the pathophysiology of Type 2 diabetes (2003) Diabetologia, 46, pp. 3-19Bray, G.A., York, D.A., Hypothalamic and genetic obesity in experimental animals: An autonomic and endocrine hypothesis (1979) Physiol Rev, 59, pp. 719-809Bray, G.A., York, D.A., The MONA LISA hypothesis in the time of leptin (1998) Recent Prog Horm Res, 53, pp. 95-117. , discussion 117-118Scomparin, D.X., Gomes, R.M., Grassiolli, S., Rinaldi, W., Martins, A.G., De Oliveira, J.C., Gravena, C., De Freitas Mathias, P.C., Autonomic activity and glycemic homeostasis are maintained by precocious and low intensity training exercises in MSG-programmed obese mice (2009) Endocrine, 36, pp. 510-517Atef, N., Ktorza, A., Picon, L., Penicaud, L., Increased islet blood flow in obese rats: Role of the autonomic nervous system (1992) Am J Physiol, 262, pp. E736-E740Leigh, F.S., Kaufman, L.N., Young, J.B., Diminished epinephrine excretion in genetically obese (ob/ob) mice and monosodium glutamate-treated rats (1992) Int J Obes Relat Metab Disord, 16, pp. 597-604Weyer, C., Salbe, A.D., Lindsay, R.S., Pratley, R.E., Bogardus, C., Tataranni, P.A., Exaggerated pancreatic polypeptide secretion in Pima Indians: Can an increased parasympathetic drive to the pancreas contribute to hyperinsulinemia, obesity, and diabetes in humans (2001) Metabolism, 50, pp. 223-230Quilliot, D., Zannad, F., Ziegler, O., Impaired response of cardiac autonomic nervous system to glucose load in severe obesity (2005) Metabolism, 54, pp. 966-974Inoue, S., Bray, G.A., The effects of subdiaphragmatic vagotomy in rats with ventromedial hypothalamic obesity (1977) Endocrinology, 100, pp. 108-114Edvell, A., Lindstrom, P., Vagotomy in young obese hyperglycemic mice: Effects on syndrome development and islet proliferation (1998) Am J Physiol, 274, pp. E1034-E1039Balbo, S.L., Mathias, P.C., Bonfleur, M.L., Alves, H.F., Siroti, F.J., Monteiro, O.G., Ribeiro, F.B., Souza, A.C., Vagotomy reduces obesity in MSG-treated rats (2000) Res Commun Mol Pathol Pharmacol, 108, pp. 291-296Balbo, S.L., Grassiolli, S., Ribeiro, R.A., Bonfleur, M.L., Gravena, C., Brito Mdo, N., Andreazzi, A.E., Torrezan, R., Fat storage is partially dependent on vagal activity and insulin secretion of hypothalamic obese rat (2007) Endocrine, 31, pp. 142-148Scheurink, A.J., Steffens, A.B., Roossien, B., Balkan, B., Sympathoadrenal function in genetically obese Zucker rats (1992) Physiol Behav, 52, pp. 679-685Barnard, R.J., Wen, S.J., Exercise and diet in the prevention and control of the metabolic syndrome (1994) Sports Med, 18, pp. 218-228Olney, J.W., Brain lesions, obesity, and other disturbances in mice treated with monosodium glutamate (1969) Science, 164, pp. 719-721Olney, J.W., Glutamate-induced neuronal necrosis in the infant mouse hypothalamus. An electron microscopic study (1971) J Neuropathol Exp Neurol, 30, pp. 75-90Martins, A.C., Souza, K.L., Shio, M.T., Mathias, P.C., Lelkes, P.I., Garcia, R.M., Adrenal medullary function and expression of catecholamine-synthesizing enzymes in mice with hypothalamic obesity (2004) Life Sci, 74, pp. 3211-3222Nardelli, T.R., Ribeiro, R.A., Balbo, S.L., Vanzela, E.C., Carneiro, E.M., Boschero, A.C., Bonfleur, M.L., Taurine prevents fat deposition and ameliorates plasma lipid profile in monosodium glutamate-obese rats (2011) Amino Acids, 41, pp. 901-908Ribeiro, R.A., Balbo, S.L., Roma, L.P., Camargo, R.L., Barella, L.F., Vanzela, E.C., Carneiro, E.M., Bonfleur, M.L., Impaired muscarinic type 3 (M3) receptor/PKC and PKA pathways in islets form MSG-obese rats (2013) Mol Biol Rep, 40, pp. 4521-4528Scomparin, D.X., Grassiolli, S., Marcal, A.C., Gravena, C., Andreazzi, A.E., Mathias, P.C., Swim training applied at early age is critical to adrenal medulla catecholamine content and to attenuate monosodium L-glutamate-obesity onset in mice (2006) Life Sci, 79, pp. 2151-2156Andreazzi, A.E., Scomparin, D.X., Mesquita, F.P., Balbo, S.L., Gravena, C., De Oliveira, J.C., Rinaldi, W., Mathias, P.C., Swimming exercise at weaning improves glycemic control and inhibits the onset of monosodium L-glutamate-obesity in mice (2009) J Endocrinol, 201, pp. 351-359Scomparin, D.X., Grassiolli, S., Gomes, R.M., Torrezan, R., De Oliveira, J.C., Gravena, C., Pera, C.C., Mathias, P.C., Low-Intensity swimming training after weaning improves glucose and lipid homeostasis in MSG hypothalamic obese mice (2011) Endocr Res, 36, pp. 83-90Delghingaro-Augusto, V., Decary, S., Peyot, M.L., Latour, M.G., Lamontagne, J., Paradis-Isler, N., Lacharite-Lemieux, M., Bergeron, R., Voluntary running exercise prevents beta-cell failure in susceptible islets of the Zucker diabetic fatty rat (2012) Am J Physiol Endocrinol Metab, 302, pp. E254-E264Balbo, S.L., Bonfleur, M.L., Carneiro, E.M., Amaral, M.E., Filiputti, E., Mathias, P.C., Parasympathetic activity changes insulin response to glucose and neurotransmitters (2002) Diabetes Metab, 28, pp. 3S13-3S17. , discussion 13S108-13S112Harms, P.G., Ojeda, S.R., A rapid and simple procedure for chronic cannulation of the rat jugular vein (1974) J Appl Physiol, 36, pp. 391-392Ribeiro, R.A., Vanzela, E.C., Oliveira, C.A., Bonfleur, M.L., Boschero, A.C., Carneiro, E.M., Taurine supplementation: Involvement of cholinergic/phospholipase C and protein kinase A pathways in potentiation of insulin secretion and Ca2+ handling in mouse pancreatic islets (2010) Br J Nutr, 104, pp. 1148-1155Bernardis, L.L., Patterson, B.D., Correlation between 'Lee index' and carcass fat content in weanling and adult female rats with hypothalamic lesions (1968) J Endocrinol, 40, pp. 527-528Pollard, H.B., Ornberg, R., Levine, M., Brocklehurst, K., Forsberg, E., Lelkes, P.I., Morita, K., Regulation of secretion from adrenal chromaffin cells (1985) Physiologist, 28, pp. 247-254Gautam, D., Han, S.J., Hamdan, F.F., Jeon, J., Li, B., Li, J.H., Cui, Y., Wess, J., A critical role for beta cell M3 muscarinic acetylcholine receptors in regulating insulin release and blood glucose homeostasis in vivo (2006) Cell Metab, 3, pp. 449-461Theintz, G.E., The endocrine impact of sports (1986) Schweiz Med Wochenschr, 116, pp. 413-418Nonogaki, K., New insights into sympathetic regulation of glucose and fat metabolism (2000) Diabetologia, 43, pp. 533-549Holloszy, J.O., Exercise-induced increase in muscle insulin sensitivity (2005) J Appl Physiol, 99, pp. 338-343. , (1985)Frosig, C., Richter, E.A., Improved insulin sensitivity after exercise: Focus on insulin signaling (2009) Obesity (Silver Spring), 17, pp. S15-S20. , 03Corcoran, M.P., Lamon-Fava, S., Fielding, R.A., Skeletal muscle lipid deposition and insulin resistance: Effect of dietary fatty acids and exercise (2007) Am J Clin Nutr, 85, pp. 662-677Miranda, R.A., Branco, R.C., Gravena, C., Barella, L.F., Da Silva Franco, C.C., Andreazzi, A.E., De Oliveira, J.C., De Freitas Mathias, P.C., Swim training of monosodium L-glutamate-obese mice improves the impaired insulin receptor tyrosine phosphorylation in pancreatic islets (2013) Endocrine, 43, pp. 571-578Zoppi, C.C., Calegari, V.C., Silveira, L.R., Carneiro, E.M., Boschero, A.C., Exercise training enhances rat pancreatic islets anaplerotic enzymes content despite reduced insulin secretion (2011) Eur J Appl Physiol, 111, pp. 2369-2374Calegari, V.C., Zoppi, C.C., Rezende, L.F., Silveira, L.R., Carneiro, E.M., Boschero, A.C., Endurance training activates AMP-activated protein kinase, increases expression of uncoupling protein 2 and reduces insulin secretion from rat pancreatic islets (2011) J Endocrinol, 208, pp. 257-264Tsuchiya, M., Manabe, Y., Yamada, K., Furuichi, Y., Hosaka, M., Fujii, N.L., Chronic exercise enhances insulin secretion ability of pancreatic islets without change in insulin content in non-diabetic rats (2013) Biochem Biophys Res Commun, 430, pp. 676-682Wang, Y.H., Hu, H., Wang, S.P., Tian, Z.J., Zhang, Q.J., Li, Q.X., Li, Y.Y., Zang, W.J., Exercise benefits cardiovascular health in hyperlipidemia rats correlating with changes of the cardiac vagus nerve (2010) Eur J Appl Physiol, 108, pp. 459-468Urano, Y., Sakurai, T., Ueda, H., Ogasawara, J., Sakurai, T., Takei, M., Izawa, T., Desensitization of the inhibitory effect of norepinephrine on insulin secretion from pancreatic islets of exercise-trained rats (2004) Metabolism, 53, pp. 1424-143